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Heterochrony and the mammalian middle ear
How might heterochrony have played a role in the evolution of the mammalian jaw and middle ear? In 2007 Luo et al. documented in the Chinese fossil Yanoconodon ossified Meckel's cartilage connecting the dentary and ectotympanic (angular). This resembles the condition in early embryonic marsupials such as Monodelphis, where the inner ear ossicles are not separated anteriorly from the dentary, though they are separated laterally (as in Yanoconodon). This leads to the hypothesis that this feature in Yanoconodon is paedomorphic. However, whether Yanoconodon is in fact paedomorphic or rather Monodelphis - taken by Luo et al. as the most primitive extant therian - is peramorphic is debatable. Development and evolution do certainly appear to mirror each other in this example, but whether heterochrony has indeed played a role in the ear relies on placement of fossils such as Yanoconodon. The ontogenetic sequence in Monodelphis mirrors the transition seen in the evolution of later cynodonts and early mammals, whereby the postdentary bones (post dentary unit - PDU), which previously formed a large part of the jaw ramus, move backwards to form what are, in modern mammals, the inner ear ossicles and the ectotympanic bone. The ear ossicles - ectotympanic, malleus, incus, and stapes - correlate to the surangular, articular, quadrate, and columella/stapes respectively in diapsids and non-mammalian cynodonts, and all but the stapes - which connected with the oval window even at the time of the synapsid-dyapsid split - have moved backwards from forming parts of the jaw to take up their new role as ear ossicles during the course of mammalian evolution from cynodonts. The homologous nature of the PDU with the ear ossicles was noticed 22 years prior to the Origin of Species in 1837 by Karl B. Reichert in Mueller's Archiv fuer Anatomie, Physiologie, und wissenschaftliche Medicin (as it was spelt at the time), displaying that a knowledge of process - in this case evolution - is not required for proper identification of pattern. The element seen ossified in Yanoconodon is, however, not any of the ear ossicles, but rather Meckel's cartilage (named after the equally illustrious Johann Meckel of Halle), which primitivaly made up a large portion of the jaw, and originates from the first branchial arch. Reichert's cartilage on the other hand originates from the second branchial arch and forms the stapes. In the early mammal Morganucodon the PDU is attached to the jaw, and situated well lateral to the middle ear, contrasting with the position in the modern Didelphis - thought the most primitive extant therian mammal - where the PDU forms the middle ear bones. Repenomamus, and early Cretaceous eutriconodont from the Liaoning formation of China (Wang et al., 2001) also shows an ossified Meckel's cartilage curving from contact with the dentary, medially to contact with the stapes and middle ear. This may again represent an example of paedomorphosis. Attachement of the Meckelian cartilage can be inferred by a groove on the dentary - this, rather than an ossified Meckel's cartilage, is what is seen in Yanoconodon, but it is absent in the modern Canis for example. Whether or not 'reattachment' of the PDU to the jaw did indeed occur is difficult to say, as the character is very variable among early mammal groups. It is probably equally possible that multiple losses occurred. One of the two must have though as the character is variable within lineages. For example, the PDU is dettached from the jaw in Hadrocodium (see below), in monotremes, in multituberculates, symmetrodonts, eupantotheres, and in therians. In morganucodonts, docodonts, and basal australosphenidans it is attached to the jaw. In eutriconodonts the situation is variable (Repenomamus and Yanoconodon are both eutriconodonts). This is the abstract from Luo et al. (2007) looking at Yanoconodon: " Detachment of the three tiny middle ear bones from the reptilian mandible is an important innovation of modern mammals. Here we describe a Mesozoic eutriconodont nested within crown mammals that clearly illustrates this transition: the middle ear bones are connected to the mandible via an ossified Meckel’s cartilage. The connected ear and jaw structure is similar to the embryonic pattern in modernmonotremes (egg-laying mammals) and placental mammals, but is a paedomorphic feature retained in the adult, unlike in monotreme and placental adults. This suggests that reversal to (or retention of) this premammalian ancestral condition is correlated with different developmental timing (heterochrony) in eutriconodonts. This new eutriconodont adds to the evidence of homoplasy of vertebral characters in the thoraco-lumbar transition and unfused lumbar ribs among early mammals. This is similar to the effect of homeobox gene patterning of vertebrae in modern mammals, making it plausible to extrapolate the effects of Hox gene patterning to account for homoplastic evolution of vertebral characters in early mammals. " As can be seen from the above, unfused lumbar ribs, and sacral ribs display similar homoplasy in mammalian evolution, with modern therians lacking these characters and having just the ribs of the rib cage, but Morganucodon for example having several unfused lumbar ribs. This patterning - as is seen in Yanoconodon - is similar to that observed in Hox 10 triple knockout mice, and therefore it appears that the transition is regulated by changes in homeobox patterning and is relatively simple to turn "off" and "on" thanks to involvement of Hox transcription factors regulating hosts of other genes. The genetic basis of movement of the PDU has not been investigated, but could plausibly be similarly simple. Point of information: Hox 10 triple knockout alters the boundary between thoracic and lumbar, whereas Hox 11 triple knockout alters lumbar versus sacral rib identities. Both Repenomamus and Yanoconodon - both eutriconodonts - have 26 thoracolumbar vertebrae, with 19-20 thoracolumbar ribs being fairly conserved in the crown Mammalia. Jeholodens however has a patterning more similar to modern therians - it is also a eutriconodont, and appears to have evolved this patterning independently. The middle ear and brain size The issues covered here link to an apparent correlation between detachment of the PDU and increased brain size. Rowe (1996) noticed that in Didelphis developmental sequences cortex growth takes place more quickly after detachment of the ear ossicles has occurred at around day 30 of ontogeny. This seemingly correlates with the pattern seen in fossil taxa, where brain size is larger in those taxa with detached PDUs, with Luo et al. (2001a) noting that the early Jurassic fossil Hadrocodium matched the pattern predicted by Rowe (1996), with its possessing a relatively large brain which correlates with detachment of the PDU. Attachment is seen in Repenomamus however, and the brain is relatively small. Repenomamus is however much larger than Hadrocodium, and allometric scaling can go some way to explaining the relative brain size of the two taxa.